* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Download Green leaf volatiles: biosynthesis, biological functions and their
History of herbalism wikipedia , lookup
Ornamental bulbous plant wikipedia , lookup
Plant tolerance to herbivory wikipedia , lookup
Historia Plantarum (Theophrastus) wikipedia , lookup
Arabidopsis thaliana wikipedia , lookup
Cultivated plant taxonomy wikipedia , lookup
Plant stress measurement wikipedia , lookup
History of botany wikipedia , lookup
Venus flytrap wikipedia , lookup
Plant disease resistance wikipedia , lookup
Plant morphology wikipedia , lookup
Plant defense against herbivory wikipedia , lookup
Plant use of endophytic fungi in defense wikipedia , lookup
Plant physiology wikipedia , lookup
Plant breeding wikipedia , lookup
Plant evolutionary developmental biology wikipedia , lookup
Plant Biotechnology Journal (2015) 13, pp. 727–739 doi: 10.1111/pbi.12368 Review article Green leaf volatiles: biosynthesis, biological functions and their applications in biotechnology Muhammad Naeem ul Hassan1,2, Zamri Zainal1,3 and Ismanizan Ismail1,3,* 1 Faculty of Science and Technology, School of Bioscience and Biotechnology, University Kebangsaan Malaysia, Bangi, Malaysia 2 Department of Chemistry, University of Sargodha, Sargodha, Pakistan 3 Institute of Systems Biology (INBIOSIS), University Kebangsaan Malaysia, Bangi, Malaysia Received 21 September 2014; revised 25 February 2015; accepted 25 February 2015. *Correspondence (Tel +60389214546; fax +603 8921 3398; emails [email protected]; [email protected]) Keywords: lipoxygenase, hydroperoxy lyase, oxylipin, jasmonic acid, tritrophic interactions. Summary Plants have evolved numerous constitutive and inducible defence mechanisms to cope with biotic and abiotic stresses. These stresses induce the expression of various genes to activate defence-related pathways that result in the release of defence chemicals. One of these defence mechanisms is the oxylipin pathway, which produces jasmonates, divinylethers and green leaf volatiles (GLVs) through the peroxidation of polyunsaturated fatty acids (PUFAs). GLVs have recently emerged as key players in plant defence, plant–plant interactions and plant–insect interactions. Some GLVs inhibit the growth and propagation of plant pathogens, including bacteria, viruses and fungi. In certain cases, GLVs released from plants under herbivore attack can serve as aerial messengers to neighbouring plants and to attract parasitic or parasitoid enemies of the herbivores. The plants that perceive these volatile signals are primed and can then adapt in preparation for the upcoming challenges. Due to their ‘green note’ odour, GLVs impart aromas and flavours to many natural foods, such as vegetables and fruits, and therefore, they can be exploited in industrial biotechnology. The aim of this study was to review the progress and recent developments in research on the oxylipin pathway, with a specific focus on the biosynthesis and biological functions of GLVs and their applications in industrial biotechnology. Introduction As plants are sessile organisms, they are constrained to use structural and chemical defences against attack, and do so without the benefit of having an animal-like immune system. Nonetheless, plants are able to mount alternative strategies for effective defence, which are comprised of constitutive, as well as inducible, mechanisms against a variety of biotic and abiotic stresses. Constitutive mechanisms include protective layers on the exterior surface of plants, such as the cell wall, wax, bark and trichomes, whereas inducible mechanisms include apoptosis, production of proteins and release of defence chemicals. Plant chemical defences are products of secondary metabolism and are not directly involved in plant growth and development; however, these chemicals perform specialized roles under specific environmental and physiological conditions. Plant secondary metabolites not only serve as key players in the plant defence system, but also they have other useful biological functions. In addition, these low molecular weight organic compounds have industrial applications and are widely used as antioxidants, colourants, fragrants and flavourants (D’Haeze and Holsters, 2002; Frydman et al., 2004; Lange and Ahkami, 2013; Verdonk et al., 2003). These chemicals are deployed by plants to prevent the potential damage caused by herbivores and various pathogens, such as bacteria, viruses and fungi. The biosynthesis of secondary metabolites occurs through several metabolic pathways and varies among plant communities, depending on the species, environment and stage of development. The oxylipin pathway is one of the most important pathways in which many defencerelated genes are activated to induce chemical defence responses, which results in the synthesis of useful secondary metabolites (Figure 1). Phyto-oxylipins are a diverse class of bioactive lipids that are derived by the oxidation of polyunsaturated fatty acids (PUFAs), mainly linoleic acid (LA, 18:2 D9, 12) and a-linolenic acid (ALA, 18:3 D9, 12, 15). This class is represented by jasmonates, divinylethers and green leaf volatiles (GLVs). Jasmonates include 12-oxo-phytodienoic acid (OPDA), jasmonic acid (JA) and methyl jasmonate (MeJA), while GLVs consist of C6 and C9 aldehydes, alcohols and their esters (Baldwin et al., 2006; Liechti and Farmer, 2006; Liechti et al., 2006; Matsui, 2006; Wasternack, 2007). Jasmonates have been found to regulate various physiological processes of plant development, such as embryogenesis, seed germination, fruit ripening and leaf senescence, but these compounds are particularly important because of their role in plant defence and host immunity (Balbi and Devoto, 2008; Heinrich et al., 2013; Kessler et al., 2004; Liechti and Farmer, 2003; Wasternack, 2007). GLVs are released under various stress conditions to aid in plant defence against herbivory and bacterial and fungal pathogens (Shiojiri et al., 2006a). In addition, GLVs are a major component of the blend of volatiles used for interplant communication (Engelberth et al., 2004; Gershenzon, 2007). Here, we review the basic components of and the recent developments in the oxylipin pathway with a specific focus on the ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd 727 728 Muhammad Naeem ul Hassan et al. Figure 1 Oxylipin pathway: Biosynthesis of Jasmonates, Divinylethers and GLVs with functions of GLVs. GLVs- green leaf volatiles, PUFAs- polyunsaturated fatty acids, LOXsLipoxygenases, AOS- allene oxide synthase, DESdivinyl ether synthase, HPL- hydroperoxide lyase, ADH- alcohol dehydrogenase. biosynthesis, biological functions and biotechnological applications of GLVs. Biosynthesis of GLVs In this section, a brief description of the substrates and the enzymes involved in the biosynthetic pathway of GLVs is presented (Figure 1). Phospholipases The degradation of membrane lipids occurs under normal conditions during physiological and developmental processes in plants and may be initiated by biotic and abiotic stresses (Wasternack, 2007). Previous studies have elucidated the role of phospholipase A (PLA) enzymes in the release of free PUFAs, which are the substrates for the oxylipin pathway. For example, DEFECTIVE ANTHER DEHISCENCE 1 (DAD1) and DONGLE (DGL) possess PLA1 activity and release ALA for the biosynthesis of JA in Arabidopsis (Hyun et al., 2008; Ishiguro et al., 2001). In addition, the Arabidopsis genome has been reported to contain genes encoding secreted phospholipase A2 (sPLA2) and a family of patatin-related phospholipase A (pPLA) genes (Ryu, 2004). sPLA2 enzymes are small, calcium-dependent and strict sn2 stereo-specific proteins, but they are not related to patatin. Patatins are potato tuber proteins that form the catalytic domain of enzymes with acyl-hydrolysing activity in bacteria, yeast, animals and plants. Patatin-related enzymes have been documented to participate in different cellular functions, including lipid mobilisation during seed germination (Scherer et al., 2010). Yang et al. (2012a) reported that pPLAs are involved in the release of free fatty acids and monoacyl glycerol through the hydrolysis of membrane glycerolipids (Yang et al., 2012a). However, further studies are needed to completely understand the mechanisms by which free PUFAs become available for the oxylipin pathway. Lipoxygenases The most important enzymes of the oxylipin pathway are a family of monomeric, nonheme iron-containing dioxygenases of approximately 100 kDa, termed lipoxygenase enzymes (LOXs, EC 1.13.11). The carboxy-terminal of the polypeptide chain is comparatively larger and possesses catalytic nonheme iron, while the amino-terminal b-barrel domain is comparatively smaller and thought to participate in regulation of the enzyme’s activity (Walther et al., 2011). Recently, a tyrosine residue in the aminoterminal domain was found to be strongly associated with the carboxy-terminal subunit and is believed to play an important role in the catalytic activity and stability of the polypeptide chain (Shang et al., 2011). Members of this family catalyse the formation of unsaturated fatty acid metabolites in both animals and plants by the regio-specific and stereo-specific addition of molecular oxygen to a (Z, Z)-1, 4-pentadiene system containing PUFAs (Andreou and Feussner, 2009; Joo and Oh, 2012). In plants, these fatty acid hydroperoxides further enter various metabolic pathways to be converted into different signalling molecules, such as GLVs and jasmonates (Farmer and Mueller, €m and Funk, 2013; Feussner and Wasternack, 2002; Haeggstro 2011; Scala et al., 2013a; Schaller and Stintzi, 2009) (Figure 1). Many studies have revealed that LOXs are localized in the chloroplast in various plant species and are associated mainly with the thylakoid membranes (Bannenberg et al., 2009; Farmaki et al., 2007; Porta et al., 2008). With the advancement of analytical techniques and functional genomics, researchers have been able to identify, clone and evaluate the role of many LOX genes from different plant species. For example, three different types of LOXs in soya bean, six in Arabidopsis thaliana, 23 in cucumber and 25 in apple have been studied for their role in plant development (Bannenberg et al., 2009; Shin et al., 2008; Vogt et al., 2013; Yang et al., 2012b). The most common substrates for plants LOXs, which are provided by lipases through the degradation of membrane lipids, are LA and ALA. Several studies have shown that LOXs are quite specific towards their substrates (Feussner and Wasternack, 2002; Liavonchanka and Feussner, 2006; Siedow, 1991). Plant LOXs have been classified into two types: 9-LOXs are referred to as type-1 and are localized outside the plastids; 13-LOXs are referred to as type-2 LOXs and harbour a plastidial transit peptide. This classification is based on the regio-specific ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739 GLVs functions and their applications 729 oxygenation of PUFAs by LOX, which can occur at C-9 or at C-13 of the hydrocarbon backbone in the case of a C-18 fatty acid (Schneider et al., 2007). Typically, one of the LOX isoforms is expressed more predominantly than the others, for example the 9-LOX gene in cucumber and the 13-LOX gene in watermelon. However, it appears that the 13-LOX pathway contributes more strongly to the overall oxylipin pathway compared with the 9-LOX pathway. 9-LOX (EC 1.13.11.58) are 741–886 amino acid proteins, that share >60% amino acid sequence identity among the subclass (Vernooy-Gerritsen et al., 1984). The existence of this enzyme has been documented in many plant species, including Arabidopsis thaliana (Bannenberg et al., 2009; Lang et al., 2008; Zheng and Brash, 2010). This enzyme catalyses the oxygenation at carbon number 9 of the hydrocarbon backbone in LA and ALA to yield (9S, 10E, 12Z)-9-hydroperoxyoctadeca-10,12-dienoic acid (9HPOD) and (9S, 10E, 12Z, 15Z)-9-hydroperoxy-10,12,15-octadecatrienoic acid (9-HPOT), respectively (Liavonchanka and Feussner, 2006). These oxygenated intermediates are then converted into biologically active compounds by downstream enzymes of the oxylipin pathway (Feussner and Wasternack, 2002) (Figure 1). The products of the 9-LOX pathway serve as key players in various developmental processes in plants. Maize ZmLOX3, a 9-LOX, plays an important role in the regulation of development and also acts as a susceptibility factor (Gao et al., 2007, 2008). In the model plant Arabidopsis thaliana, 9-LOX is involved in late root development (Vellosillo et al., 2007). The induction of a specific 9-LOX gene has been reported to participate in potato tuber growth, and a reduction in tuber size was observed in response to the suppression of this gene using an antisense strategy (Kolomiets et al., 2001). Numerous previous studies have highlighted the roles of 9-LOX products in plant defence strategies, particularly in the hypersensitive response (HR). The HR is one of the first and most efficient resistance reactions and is characterized by the rapid death of plant cells in the vicinity of a pathogen attack (Cacas et al., 2005; Gobel et al., 2003; Jalloul et al., 2002; Marmey et al., 2007; Rance et al., 1998; Rusterucci et al., 1999; Sayegh-Alhamdia et al., 2008). In a recent study, Arabidopsis thaliana LOX1 (9-LOX) and DOX1 (a-Dioxygenase) were shown to possess strong antibacterial activity. Individual mutants lox1 and dox1 and a double mutant lox1dox1 were tested to evaluate their efficacy against Pseudomonas syringae pv. tomato (Pst) infection. The lox1 plants exhibited an enhanced susceptibility to the virulent strain Pst DC3000, and systemic acquired resistance (SAR) was partially impaired in both mutants. In the lox1dox1 double mutant plants, both the above-mentioned defects were further enhanced. However, pretreatment of these plants with 9-LOX and a-DOX resulted in the production of oxylipins, particularly 9-ketooctadecatrienoic acid, and protected the plant tissues against bacterial infection (Vicente et al., 2012). The activation of a 9-LOX gene in pepper (Capsicum annuum), designated as CaLOX1, has been reported to positively regulate broad-spectrum resistance and cell death in response to pathogen infection (Hwang and Hwang, 2010). Two closely related 9-LOX paralogs in maize, that is ZmLOX4 and ZmLOX5, respond to various threats, such as insects, herbivory, wounding and pathogen infection, through a unique mechanism (Park et al., 2010). 13-LOX (EC 1.13.11.12) is a subclass of the LOX family of enzymes that contains 896 to 941 amino acids. A large variety of plants have been reported to express 13-LOX genes, including soya bean, cucumber, maize and Arabidopsis thaliana (Acosta et al., 2009; Bannenberg et al., 2009; Chohany et al., 2011; Rudolph et al., 2011). This LOX family subclass is characterized by the oxygenation of carbon number 13 in the PUFA substrates LA and ALA to form (9Z, 11E, 13S)-13-hydroperoxyoctadeca-9, 11-dienoic acid (13-HPOD) and (9Z, 11E, 15Z)-13-hydroperoxyoctadeca-9, 11, 15-trienoic acid (13-HPOT). The conversion of these oxidized fatty acids to biologically active oxylipins, such as jasmonates, GLVs and divinylethers, occurs via seven different metabolic pathways (Andreou et al., 2009; Feussner and Wasternack, 2002; Gigot et al., 2010). These downstream products of 13-LOX metabolism serve as important components in the regulation of gene expression for plant defence (Farmer et al., 2003). One of the most studied and well-characterized compounds in the oxylipin pathway is the plant hormone JA, which is formed in the leaves in response to wounding and other stimuli (Feussner and Wasternack, 2002; Halitschke and Baldwin, 2003). 13-HPOT, which is generated by 13-LOX oxygenation of LA or ALA, undergoes allene oxide synthase (AOS) catalysis to form allene oxide intermediates (Tijet and Brash, 2002). Further reactions in the JA synthesis pathway are catalysed by allene oxide cyclase and 12-oxopendienoic acid (OPDA) reductase, followed by 3 cycles of b-oxidation (Andreou and Feussner, 2009). Alternatively, 13-hydroperoxide lyase (13-HPL) enzymes catalyse the conversion of 13-hydroperoxide intermediates to 6carbon aldehydes, which are believed to possess signalling functions and play a direct role in plant defence (Bate and Rothstein, 1998; Croft et al., 1993). Previously, 13-HPOT and 13hydroxytridecanoic acid (13-HOT) were described as antifungal compounds and suggested for disease control in brassica plants (Graner et al., 2003). In a recent study, 13-hydroperoxides from papaya seedlings exhibited antifungal activity against Phytophthora palmivora by inhibiting the germination of sporangia and the growth of mycelia (Sujatha et al., 2012). Certain LOXs can produce both 9- and 13- hydroperoxy metabolites; for example, LOX1, LOX2 and LOX3 in soya bean can produce 9- and 13HPODs at different pH values (Axelrod, 1981). In a recent study, 9-LOX from Nicotiana benthamiana (Nb9-LOX) was shown to possess the specificity of both 9- and 13-LOX, with a high predominance for the 9-LOX function. In this study, Nb9-LOX was incubated with LA and 13-HPL from watermelon or 9/13-HPL from melon, followed by LC–MS analysis of the products (Huang and Schwab, 2011). Hydroperoxide lyases Hydroperoxide lyase (HPL) is a member of the CYP74 subfamily of the cytochrome P450 family of enzymes. Three types of enzymes, that is AOS, HPL and divinylether synthase (DES), are included in the CYP74 subfamily, and the AOS and HPL genes have been found in all sequenced plant genomes (Brash, 2009; Hughes et al., 2009). The genes encoding HPL are found mainly in algae, mushrooms, Penicillium and higher plants and have been characterized and cloned in many plant species, such as cucumber, green bell pepper, tomato and alfalfa (Atwal et al., 2005; mez et al., 2010; Wan Noordermeer et al., 2000; Santiago-Go et al., 2013). Most HPLs are membrane bound; HPLs in plants such as Arabidopsis contain a chloroplast transit peptide, whereas HPLs in other plants, such as tomato and melon, do not have a clear transit peptide and are suggested to be microsome localized (Bate et al., 1998; Froehlich et al., 2001; Noordermeer et al., 2001). The structural details of plant HPLs remain poorly understood and require further investigation. However, recent studies have highlighted the structural aspects of HPLs in plants. For example, the green bell pepper HPL is composed of 480 ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739 730 Muhammad Naeem ul Hassan et al. amino acids and has a molecular weight of approximately 55 kDa. Circular dichroism analysis demonstrated that the protein secondary structure of dodecyl maltoside is composed of approximately 13% a-helix, 32% b-sheet, 21% turn and 31% mez et al., unordered coils (Panagakou et al., 2013; Santiago-Go 2010). Similarly, the Solanum tuberosum HPL is a protein of approximately 54 kDa (Mu et al., 2012). The functional enzyme is a trimer or a tetramer with an optimum pH range of 6–9.5 and an optimum temperature of approximately 30 °C (Gigot et al., 2010). Depending on the specificity of the substrate, plant HPLs have been classified into three types: 9-HPL, 13-HPL and 9/13 HPL (Morant et al., 2003). The majority of plant HPLs are specific for 13-hydroperoxide substrates, while enzymes from a few plant species (e.g. almond) catalyse the cleavage of 9-hydroperoxides (Mita et al., 2005). However, the HPLs from the 9/13 HPL subclass that can utilize both 9- and 13-hydroperoxide substrates have recently been documented in certain plants, such as cucumber, rice, Medicago spp. and grape (Chehab et al., 2006; De Domenico et al., 2007; Matsui et al., 2000; Zhu et al., 2012). HPLs catalyse the isomerisation of 9- and 13-hydroperoxides of PUFAs, formed by the action of 9- and 13-LOXs, respectively, to unstable hemiacetals (Grechkin et al., 2006). In the 9-HPL pathway, these hemiacetals spontaneously decompose to yield volatile C9 aldehydes, including cis-3-nonenal, trans-2-nonenal and nonvolatile C9 oxoacids. In the 13-HPL pathway, fatty acid hydroperoxide substrates undergo homolytic isomerisation between C12 and C13 to produce unstable hemiacetals, which spontaneously decompose to release volatile C6 aldehydes, hexanal and (Z)-3-hexenal from LA and ALA, respectively (Grechkin and Hamberg, 2004). Nonvolatile C12 oxoacids are also formed in these reactions, for example 12-oxo-(Z)-9-dodecenoic acid, which is a precursor of traumatin. These aldehydes are the parent compounds for all other C6 aldehydes, C6 alcohols and their acetylated derivatives (D’Auria et al., 2007; Galliard et al., 1976; Hatanaka, 1993; Shiojiri et al., 2006b). The conversion of aldehydes to alcohols is brought about by NAD-dependent alcohol dehydrogenase (ADH) to confer higher stability (Fauconnier et al., 1999). All of these saturated and unsaturated C6/C9 aldehydes, alcohols and esters, which are synthesized in vegetative plant tissue, particularly the leaves are volatile and are collectively referred to as GLVs. GLVs are released within seconds in response to tissue disruption due to biotic or abiotic stresses as a result of activation of the HPL genes (Figure 1). Biological functions of GLVs Different roles of GLVs in plant defence, communication and natural aromas and flavours are presented in this section (Table 1). GLVs in plant defence To maintain a healthy flora, phyto-artillery has to confront against multiple intruders at many fronts. Oxylipin pathway is also a component of these frontline defence mechanisms that is activated in response to various threats, including pathogens and herbivory (Figure 1). The phytohormone JA has been studied extensively to determine its efficacy and mechanism in plant defence against biotic threats. Currently, JA is considered one of the major phytohormones involved in plant defence, together with salicylic acid and ethylene, due to its role in inducing resistance against necrotrophic pathogens, chewing herbivores and certain phloem-feeding insects. Other jasmonates, including OPDA, methyl jasmonate and L-isoleucine jasmonate, have also gained attention in recent years for their importance in stress signalling and SAR. As the scope of the present review is to highlight the role of another component of the oxylipin pathway, readers are referred to recently published review articles for a comprehensive description of JA (De Vleesschauwer et al., 2013; Derksen et al., 2013; Lyons et al., 2013; Wasternack and Hause, 2013; Yang et al., 2013). The GLV/HPL pathway has recently been implicated in plant defence and is less well understood than the JA/AOS pathway. GLVs serve as signals of stress within a plant as well as between neighbouring plants within a plant community. Plants emit only trace amounts of the GLVs under normal physiological conditions; however, under stressed conditions, these volatiles can be formed very rapidly (Allmann and Baldwin, 2010; D’Auria et al., 2007). Increased synthesis and emission of these compounds has been reported under stress-related conditions such as herbivory, pathogen attack and abiotic stimuli (Brilli et al., 2011; Fall et al., 1999; Gomi et al., 2003; Heiden et al., 2003; Shiojiri et al., 2006a; Turlings et al., 1995). However, numerous studies have suggested that the two competing branches of the oxylipin pathway crosstalk during metabolism and the stress response. In a recent study, Christensen et al. (2013) highlighted the role of ZmLOX10, a Zea mays LOX that provides substrates for GLV biosynthesis, and the coordination between the GLV and JA pathways in the defence of maize plants against insect herbivory (Christensen et al., 2013). In addition, Liu et al. (2012) recently reported that the AOS and HPL branches of the oxylipin pathway crosstalk in a coordinated manner to manipulate disease resistance in rice (Liu et al., 2012). Similarly, pretreatment of Arabidopsis plants with aldehyde GLVs, particularly (E)-2-hexenal, enhanced the sensitivity of the plants towards methyl-jasmonate (Hirao et al., 2012). An HPL gene (OsHPL3) in rice plants was recently shown to modulate direct and indirect plant defences against various biotic threats by affecting the JA and GLV levels (Tong et al., 2012). GLVs in plants priming and herbivore defence Insect herbivores utilize the physical and chemical resources of the host plants for feeding and oviposition. Generalist herbivores can use a variety of plant species from various families for feeding purposes, but specialist herbivores have only one or a few options for feeding. In response to herbivory, plants produce direct defence molecules, which act as toxins and repellents, as well as indirect defence molecules, such as GLVs and extra-floral nectar, which attract the natural enemies of herbivores. Interplant communication via airborne signalling is now a well-established phenomenon in plant science, but it remained a controversial topic for many years. The debate over ‘talking trees’ began in the 1980s, and over the last three decades, researchers have accumulated significant evidence to support this hypothesis. It is now a relatively well-established theory that plants ‘eavesdrop’ on a bouquet of volatile organic compounds (VOCs), of which GLVs and terpenoids are the major constituents. The bouquet of volatiles is released by plants, that is the emitters, in the plant headspace and then into the atmosphere in response to biotic or abiotic stresses. These volatile signals are carried by the air to neighbouring plants, that is the receivers, which perceive the signal and respond by activating the expression of genes related to direct and indirect defences (Baldwin et al., 2006; Heil, 2014; Kessler et al., 2006). ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739 GLVs functions and their applications 731 Table 1 Biological functions of GLVs Biological functions GLVs involved/tested Description/comments Reference Herbivore (E)-2-hexenal and 3-hexen-1-ol Volatile extracts from cucumber, cotton, tomato, tobacco, cabbage and celery were Li et al. (2014) defence used to evaluate the behavioural responses of Bemisia tabaci (E)-2-hexenal and (Z)-3-hexenyl acetate (Z)-3-hexenal GLVs released in response to damage caused by herbivory were shown to attract the Shiojiri et al. (2006b) parasitic wasp, Cotesia glomerata, that attacks Pieris rapae larvae The role of a rice HPL gene (OsHPL3) in resistance against white-backed Wang et al. (2014) planthopper is reported GLVs blend The involvement of rice OsHPL3 in direct and indirect defences against insect Tong et al. (2012) herbivores is highlighted Nonanal Tritrophic interactions: Colorado Potato Beetle (CPB)-infested potato plants Gosset et al. (2009) released GLVs, particularly nonanal, that serve as an attractants for predators of the CPB (Z)-3-hexenol Activation of defence responses by GLVs against insect herbivory is reported Engelberth et al. (2013) in maize plants (Z)-3-hexenol Role by which (Z)-3-hexenol and its acetylated derivative activate defences Farag et al. (2005) against insect herbivory is elucidated Hexenyl acetate Tritrophic interactions: Indirect defence mechanisms mediated by wound-inducible Chehab et al. (2008) volatile signals to attract the natural enemies of plant invaders GLVs blend Tritrophic interactions: Tobacco plants reduced their herbivore load by releasing Halitschke et al. (2008) GLVs and terpenoids for attracting predatory bugs (Z)-3-hexenol Tritrophic interactions: (Z)-3-hexenol released from leafminer pests, Liriomyza Wei et al. (2007) huidobrensi-damaged plants attracted a naive parasitic wasp, Opius dissitus, for rescue (E)-2-hexenal Tritrophic interactions: treatment of soya bean plants at early flowering stages Vieira et al. (2014) with synthetic (E)-2-hexenal attracted Trissolcus spp and other natural enemies of stink bugs (E)-2-hexenal, (E-2, Z-6)nonadienal and (E)-2-nonenal Plants (E)-2-hexenal priming The toxicity of GLVs was tested against three medically significant mites and Hubert et al. (2008) pests, and the inhibitory concentrations were optimized Bouquet of volatiles from clipped sagebrush, including (E)-2-hexenal, successfully Kessler et al. (2006) primed the tobacco trypsin proteinase inhibitor response (E)-2-hexenal Increased sensitivity of Arabidopsis plants to MeJA was observed Hirao et al. (2012) Nonanal Priming of lima bean plants through induction of LOX and PR-2 gene expression Yi et al. (2009) (Z)-3-hexenal, (Z)-3- hexenol Priming of corn plants due to herbivorous insects reported Engelberth et al. (2004) Acetylated derivatives released by GLVs in intact maize plants induced the priming Yan and Wang (2006) via airborne signalling and (Z)-3-hexenyl acetate (Z)-3-hexenyl acetate of neighbouring plants GLVs blend The intensity of GLVs and the frequency of exposure were optimized for priming Shiojiri et al. (2012) Arabidopsis plants Pathogen defence (E)-2-hexenal and (Z)-3-hexenyl Antifungal activity of GLVs against Botrytis cinerea identified Shiojiri et al. (2006a) Defence against the fungal pathogen, Aspergillus carbonarius was indicated by the Mita et al. (2007) acetate C9 aldehydes induction of 9LOX/HPL gene expression, producing C9 aldehydes in immature almond seeds Mixture of oxylipins The large-scale screening of oxylipins for their antimicrobial activity against several Prost et al. (2005) plant pathogens was reported (E)-2-hexenal Fungal protein targets for C6 aldehydes were elucidated using radio-labelled Myung et al. (2007) aldehydes in Botrytis cinerea C9 aldehydes Fungicidal action against fungal pathogens, Botrytis cinerea and Fusarium oxysporum Matsui et al. (2006) was reported due to 9/13 HPL activity in cucumber Constitutive and wound induced GLVs including (Z)- An HPL from tea, overexpressed in tomato revealed enhanced resistance against Xin et al. (2014) the fungal pathogen, Alternaria alternata f. sp. Lycopersici hexenal and (Z)-3-hexen-1-ol (E)-2-hexena1, (Z)-3-hexeno1 One of the earliest reports on the bactericidal activity of GLVs Croft et al. (1993) (E)-3-hexenal Bactericidal potential of various GLVs tested against different organisms. (E)-3-hexenal Nakamura and was found to be the most efficient compound against many bacteria Hatanaka (2002) Kishimoto et al. (2008) ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739 732 Muhammad Naeem ul Hassan et al. Table 1 Continued Biological functions GLVs involved/tested Description/comments (Z)-3-hexenal, (E)-2-hexenal, Transgenic Arabidopsis plants with an overexpressed or suppressed HPL gene were and n-hexanal Reference studied to show that C6 aldehydes have direct fungicidal activity against Botrytis cinerea Aroma and flavour C6 and C9 aldehydes and alcohols Changes in the contents of various GLVs were detected during the course of Wan et al. (2013) cucumber fruit ripening (Z)-3-hexen-1-ol, 1-hexanol, hexanal, (E)-2-hexenal and Progressive replacement of the green odour with floral and sweet sensations due to Oliveira et al. (2011) changes in the levels of GLVs was reported during strawberry fruit ripening hexyl acetate Hexanal, (E)-2-hexenal, hexanol and (Z)-3-hexenol Hexanal and (E)-2-hexenal were found to be the major volatiles in the green Velickovic et al. (2013) Medlar fruit, and hexenol and (Z)-3-hexenol were the major volatiles present in the ripe fruit GLVs blend Flavour- and aroma-active compounds reported in different brands of tea Alasalvar et al. (2012) (E)-2-Hexenal Two strawberry cultivars were analysed to determine the major active odour Du et al. (2011) volatiles. (E)-2-hexenal was found to be the major volatile for ‘fresh strawberry’ flavour (Z)-3-hexenal and (E)- 2-hexenal Profiling of the aroma components in fresh cherry tomato revealed (Z)-3-hexenal Selli et al. (2014) and (E)-2-hexenal to be the major aroma-active compounds, with strong green grassy and green-leafy odour, respectively As a major component of herbivore-induced plant volatiles (HIPVs), GLVs participate in indirect defence via tritrophic interactions and priming, a process by which HIPVs from a damaged plant prepare neighbouring plants to defend themselves against a future attack (Frost et al., 2008; Goellner and Conrath, 2008) (Table 1). Herbivore dynamics may be influenced by antiherbivore defence priming through the activation of direct and indirect defence mechanisms via tritrophic interactions (Kaplan, 2012). However, the amount of volatiles released from plant foliage in response to herbivory or pathogen stresses is directly related to the severity of the attack (Niinemets et al., 2013). In a recent report, Shiojiri et al. (2012) optimized the concentration of GLVs released by damaged Arabidopsis plants and the frequency of exposure to neighbouring undamaged plants, which was required for successful defence priming (Shiojiri et al., 2012). Mechanical wounding of plants or attack by herbivores activates the oxylipin pathway and initiates the synthesis of GLVs. The emission of GLVs in response to herbivory induces indirect defences by activating defence-related gene expression and attracting carnivorous arthropods to locate the herbivores (Halitschke et al., 2008). The up-regulation of numerous genes involved in direct and indirect defences has been documented in maize plants exposed to (Z)-3-hexenol. Furthermore, it was demonstrated that (Z)-3-hexenol is a much more powerful elicitor of defences against insect herbivory compared with common defence signals, such as methyl jasmonate, methyl salicylate and ethylene (Engelberth et al., 2013). Recent studies have elucidated the role of insect oral secretions in promoting wound-induced responses (Erb et al., 2012; Meldau et al., 2012). For example, herbivore-damaged lima bean plants produced volatiles that triggered the production of extra-floral nectar in undamaged plants. Predatory arthropods are attracted by extra-floral nectar, which represents an induced defence mechanism (Heil and Kost, 2006; Heil and Silva Bueno, 2007). Resistance against bacterial blight in rice plants is induced by white-backed planthopper (Sogatella furcifera) (Gomi et al., 2010). Maize plants treated with three GLVs, that is, (Z)3-hexenal, (Z)-3-hexen-1-ol, and (Z)-3- hexenyl acetate, subsequently produced higher concentrations of JA than the control plants. Furthermore, the production of HIPVs in GLV-treated plants was enhanced in response to caterpillar regurgitant combined with mechanical wounding (Engelberth et al., 2004). The same GLVs were later shown to up-regulate the expression of three genes of the octadecanoid pathway for the synthesis of JA (Engelberth et al., 2007). Similarly, priming of HIPV emission and up-regulation of defence gene expression was observed in undamaged maize plants exposed to Spodoptera littoraliswounded conspecifics. Moreover, Spodoptera littoralis had lower relative growth rates after feeding on primed maize plants, and the bouquet of HIPVs released from these plants was more attractive for the parasitic wasp Cotesia marginiventris (von M erey et al., 2013; Ton et al., 2007). (Z)-3-hexenol, a universal GLV induced by mechanically-damaged or leafminer-damaged plants, is suggested to be the most important general damage attractant that helps parasitoids locate their prey or the host plant (Wei et al., 2007). Arabidopsis plants overexpressing HPL but with suppressed AOS (aos-OX-HPL) released higher amounts of volatile hexenyl acetate following aphid (Myzus persicae) infestation. Furthermore, the results of a choice assay indicated that female Aphidius colemani, a parasitic wasp, were more attracted to GLVs produced by these plants after mechanical damage than the plants in which both AOS and HPL were silenced (aos-hpl) and therefore unable to release hexenyl acetate or any other GLV (Chehab et al., 2008). Overexpression of the bell pepper (Capsicum annuum L.) HPL gene in Arabidopsis plants renders the plants more attractive to the parasitic wasp Cotesia glomerata due to their enhanced production of GLVs. By contrast, the transgenic Arabidopsis plants in which HPL was suppressed by antisense cloning of the gene could not produce significant amounts of GLVs and were less attractive to parasitoids, which resulted in reduced resistance to herbivory (Shiojiri et al., 2006a). In a recent study, the antisense expression of a rice HPL (OsHPL3) ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739 GLVs functions and their applications 733 highlighted the role of one of the GLVs, that is, (Z)-3-hexenal, in the resistance of rice plants against the white-backed planthopper (Wang et al., 2014). GLVs in pathogen defence Plant pathogens have been classified as either necrotrophs that kill plant cells before feeding on the dead plant tissue or as biotrophs that use living plant tissue for nutritional purposes without causing any damage. To restrict the invasion and spread of potential microbial pathogens, plants have evolved different mechanisms as a part of their local defence and SAR strategies. Several studies have highlighted the role of oxylipins in plant defence against a variety of pathogens (Table 1). Prost et al. (2005) screened numerous oxylipins for antimicrobial activity and found that most of the oxylipins were active against eukaryotic microbes (Prost et al., 2005). In an earlier study, two GLVs, that is (E)-2-hexenal and (Z)-3-hexenol, exhibited bactericidal activity at low and high concentrations, respectively (Croft et al., 1993). In another study, the antibacterial activity of GLVs was reported against both Gram-positive and Gram-negative bacteria (Nakamura and Hatanaka, 2002). The priming of plant resistance against a pathogenic bacterium due to airborne plant-plant signalling was recently reported. A natural population of lima beans (Phaseolus lunatus) growing adjacent to conspecific neighbours that had been chemically induced with benzothiadiazole was more resistant to infection by the bacterial pathogen Pseudomonas syringae pv. syringae. Nonanal was identified as the major constituent in the headspace of the plants treated with benzothiadiazole, and the enhanced expression of genes related to PATHOGENESISRELATED PROTEIN2 (PR-2), which are likely involved in this effect, was observed (Yi et al., 2009). Treatment with (E)-2-hexenal or the presence of active HPL enhanced the susceptibility of Arabidopsis plants to Pseudomonas syringae pv. tomato. This response was mediated by ORA59, a key transcription factor in the JA pathway (Scala et al., 2013b). Fungicidal activity was detected in Arabidopsis thaliana plants overexpressing the HPL gene in response to the accumulation of higher amounts of C6 aldehydes following infection with the plant pathogen Botrytis cinerea. However, suppression of this gene resulted in reduced amounts of C6 aldehydes compared with the wild type plants, and therefore less resistance to the fungal pathogen (Kishimoto et al., 2008). In another study, the antifungal activity of the infection site was monitored using radiolabelled C6 aldehydes that were synthesized in vitro from ALA using LOX and HPL extracts and Botrytis cinerea. Most of the radio-labelled C6 aldehydes were recovered from the fungal surface proteins and mainly from the conidia rather than the mycelia (Myung et al., 2007). Matsui et al. (2006) documented the fungicidal activities of C6 and C9 aldehydes against two fungal pathogens, Botrytis cinerea and Fusarium oxysporum, in disrupted cucumber leaves (Matsui et al., 2006). A recent study reported enhanced resistance of transgenic tomato plants with constitutively expressed tea HPL against the necrotrophic fungus Alternaria alternata f. sp. lycopersici (Xin et al., 2014). Certain GLVs, such as hexanal and (E)-2-hexenal, have been implicated in food storage due to their antimicrobial activities (Hubert et al., 2008). GLVs in natural aromas and flavours Humans can sense more than 7000 volatile compounds with the use of 347 olfactory receptors (Goff and Klee, 2006). A complex mixture of more than 1000 volatile compounds that include aldehydes, alcohols, esters, terpenes, and some carbonyl and sulphur compounds impart aroma to fruits (Lara et al., 2003). Plant volatiles serve as a source of relief and refreshment for humans due to their aromas and odours, which is indicative of absence of insects and harmful microorganisms (Table 1). Consumers’ choice of fruits, vegetables and processed foods depends mainly on a blend of characteristics such as aroma, colour, odour and flavour. Volatile compounds are synthesized in the vegetative tissues of plants in response to biotic stresses, mainly herbivory and pathogens (Arimura et al., 2009). The disruption of glandular trichomes due to herbivory results in the emission of volatile compounds at high concentrations to repel the attackers (Schilmiller et al., 2008). These volatile compounds are important constituents of the flavour and fresh green aroma in fruits and vegetables and impart a characteristic odour to each plant referred to as the ‘green note’ (Gigot et al., 2010; Hatanaka, 1993; Weichert et al., 2002). Volatile profiling of strawberry (Arbutus unedo) fruit during different stages of ripening showed that C6 alcohols are the major components of the blend of volatiles, followed by aldehydes and esters, until the final ripening stage (Oliveira et al., 2011). The key aromatic compounds that contribute to the green, grassy odour note of guava fruit are (Z)-3-hexenal and hexanal (Steinhaus et al., 2009). The volatile alcohols, (Z)-2-hexenol and (Z)-3-hexenol, and the aldehydes hexanal and (E)-2-hexenal, with their green, grassy, sweet, fruity odour, are the major contributors of the sensory characteristics in different tea varieties (Alasalvar et al., 2012; Borse et al., 2002; Schuh and Schieberle, 2006; Wang et al., 2011). An analysis of odourants from strawberry indicated that ethyl hexanoate is one of the most intense volatile esters that impart a fruity aroma (Du et al., 2011). In a recent study, (Z)-3-hexenal and (E)-2-hexenal were identified as the most powerful aromatic active volatiles in fresh cherry tomato extracts (Selli et al., 2014). Applications of GLVs in biotechnology Natural flavour compounds share a major part of the global market of food additives. Green note products were valued at approximately 900 million USD in the worldwide market in 2006 and have continued to increase steadily (Xu et al., 2007). Consumers’ demand for natural flavourants and odourants has increased in recent years due to health and safety concerns. The advancement of knowledge has led to new strategies for the large-scale production of these natural food additives through biotechnological applications. Because of the blend of inherent green, fresh and fruity aromas, GLVs are widely applied in the food and beverage industry (Fukushige and Hildebrand, 2005) (Table 2). The natural ‘fresh green’ aroma of fruits and vegetables, which is lost during industrial processing, is reconstituted through the application of HPL-generated volatiles (Delcarte et al., 2003). Buchhaupt et al. (2012) described a highly efficient process for the synthesis of green note by overexpressing soya bean LOX2 and watermelon HPL in the yeast Saccharomyces cerevisiae (Buchhaupt et al., 2012). The production of large quantities of hexanal, (Z)-3-hexenal and (E)-2-hexenal was achieved by designing an efficient biosynthetic strategy. A viral vector system was used in this design to overexpress a 13-LOX gene from soya bean (GmVLXC) and a 13-HPL gene from watermelon (ClHPL) by agroinfiltration in Nicotiana benthamiana and incubating the plant leaf extract with LA (Huang et al., 2010). Using the same ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739 734 Muhammad Naeem ul Hassan et al. Table 2 Applications of GLVs in biotechnology Plant/fruit (enzyme source) Target GLVs Process description Reference HPL from Amaranthus tricolor (E)-2-hexenal Synthesis and purification of (E)-2-hexenal, by salt-adding steam Xiong et al. (2012) distillation is described HPL from sugar beet (E)-2-hexenal Modulated substrate addition and continuous products removal employed Gigot et al. (2012) for the efficient biotransformation of fatty acid hydroperoxide substrates to GLVs Pink guava fruit (Z)-3-hexenal and hexanal 13-LOX gene from Soya bean (GmVLXC) and a 13-HPL Hexanal, (Z)-3- hexenal and (E)-2-hexenal gene from watermelon 9-LOX/9-HPL, 9-LOX/tomato Re-engineering of aroma- and odour-active compounds and omission tests Steinhaus et al. (2009) employed for the characterisation of guava fruit aroma Production of large amounts of C6 aldehydes by expressing a viral vector Huang et al. (2010) containing soybean LOX and watermelon HPL in Nicotiana benthamiana plants is described C9-aldehydes The biotransformation of LA to C9 aldehydes and trihydroxy fatty acids peroxygenase and 9-LOX/potato using tobacco leaf extracts is described. The tobacco plants contained epoxide hydrolase a recombinant viral vector with genes encoding enzymes downstream Huang and Schwab (2012) of 9-LOX from different sources by agrobacterium infiltration strategy, C9-aldehydes and trihydroxy fatty acids were produced in large quantities by 9-LOX/9-HPL, 9-LOX/tomato peroxygenase and 9-LOX/potato epoxide hydrolase overexpression (Huang and Schwab, 2012). Gigot et al. (2012) devised a bioreactor for the synthesis of original GLVs from 13-HPOT using recombinant sugar beet HPL (BVHPL). This process was highly efficient, and the product, that is a mixture of GLVs with (Z)-3-hexenal and (E)-2-hexenal as the major constituents, was suggested to be of high quality and suitable for use in foods and beverages as a natural aroma (Gigot et al., 2012). Similarly, (E)-2-hexenal has been synthesized from 13-HPOT and Amaranthus tricolor HPL using a green method, followed by purification using salt-adding steam distillation (Xiong et al., 2012). Conclusion and future prospects In the last few decades, numerous studies have reported on the role of the oxylipin pathway in plant physiology and defence. As discussed earlier in this review, a number of stresses can activate the oxylipin pathway, resulting in the release of higher amounts of jasmonates and GLVs, which are otherwise released in very low concentrations (Allmann and Baldwin, 2010). The release of higher GLV concentrations under stressed conditions led us to conclude that gene expression for the GLV biosynthetic pathway is induced by signals from infection or stress. However, the nature of these signals and the mechanisms by which these stress signals lead to the generation of the defence response remain elusive, particularly the release of free or esterified PUFAs. New strategies need to be devised and certain novel substrates may need to be designed and tested to identify the ‘missing link’ between the perception of stress and the defence response in the affected plants. The importance of GLVs in the plant response to microbial pathogen attack has been studied since the early 1990s. Although many studies have shown encouraging results, most are limited to laboratory experiments that were performed using synthetic GLVs. Further laboratory and field experiments using the natural bouquet of these volatiles are required to comprehensively understand this process. The most interesting aspect of the ongoing research on GLVs is their role in tri-trophic interactions and plant-plant communication, where these compounds have emerged as key players. Optimistically, it appears that we are close to entering an era of understanding ‘plant psychology’, where GLVs play a central role, similar to the nerve impulses in the human central nervous system. Currently, most of our knowledge on plant-insect interactions is limited to only a few plant species, and the molecular mechanisms driving these processes are not clear (Broekgaarden et al., 2011). However, an extensive amount of research from different fields in the plant and biological sciences should be integrated to understand the language that plants use for communication within their ecosystem. Laboratory and field experiments may be designed to evaluate and analyse these signals at the genomics, proteomics and metabolomics levels to answer certain questions. For example, what types of signals are involved in stress and the associated response? What types of plants in an ecosystem transmit signals and what types of plant receptors can receive airborne signals? How are the signals transmitted through receiver plants, and how do they induce a pre-attack defence response? The best solution to these questions will likely arise from a more intensive and systematic approach that uses systems biology and an integrative biology platform. In addition, we need a comprehensive understanding of the signalling mechanisms of these pathways at the genetic and molecular levels. The modification of key steps in these pathways using genetic engineering tools and more advanced biochemical strategies, such as epigenetic alterations, could be used to firmly control the pathway switches (Seymour et al., 2013). Enabling useful plants to produce their own herbicides, pesticides and antimicrobials will help us eliminate the need for toxic sprays, reduce costs and protect the environment. This strategy could be helpful for the protection of crops and normal flora as well as the production of natural foods with improved quality. Acknowledgement We would like to thank and show our appreciation to Universiti Kebangsaan Malaysia for financing this project through “Research University Grant (DLP-2013-008). References Acosta, I.F., Laparra, H., Romero, S.P., Schmelz, E., Hamberg, M., Mottinger, J.P., Moreno, M.A. and Dellaporta, S.L. (2009) tasselseed1 is a lipoxygenase ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739 GLVs functions and their applications 735 affecting jasmonic acid signaling in sex determination of maize. Science, 323, 262–265. Alasalvar, C., Topal, B., Serpen, A., Bahar, B., Pelvan, E. and Gokmen, V. (2012) Flavor characteristics of seven grades of black tea produced in Turkey. J. Agric. Food Chem. 60, 6323–6332. Allmann, S. and Baldwin, I.T. (2010) Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science, 329, 1075– 1078. Andreou, A. and Feussner, I. (2009) Lipoxygenases – structure and reaction mechanism. Phytochemistry, 70, 1504–1510. Andreou, A., Brodhun, F. and Feussner, I. (2009) Biosynthesis of oxylipins in non-mammals. Prog. Lipid Res. 48, 148–170. Arimura, G., Matsui, K. and Takabayashi, J. (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol. 50, 911–923. Atwal, A.S., Bisakowski, B., Richard, S., Robert, N. and Lee, B. (2005) Cloning and secretion of tomato hydroperoxide lyase in Pichia pastoris. Process Biochemistry, 40(1), 95–102. Axelrod, B. (1981) Lipoxygenase from soybeans. Methods Enzymol. 71, 441– 451. Balbi, V. and Devoto, A. (2008) Jasmonate signalling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytol. 177, 301–318. Baldwin, I.T., Halitschke, R., Paschold, A., von Dahl, C.C. and Preston, C.A. (2006) Volatile signaling in plant-plant interactions: “talking trees” in the Genomics Era. Science, 311, 812–815. Bannenberg, G., Martinez, M., Hamberg, M. and Castresana, C. (2009) Diversity of the enzymatic activity in the lipoxygenase gene family of Arabidopsis thaliana. Lipids, 44, 85–95. Bate, N.J. and Rothstein, S.J. (1998) C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J. 16, 561–569. Bate, N.J., Sivasankar, S., Moxon, C., Riley, J.M., Thompson, J.E. and Rothstein, S.J. (1998) Molecular characterization of an Arabidopsis gene encoding hydroperoxide lyase, a cytochrome P-450 that is wound inducible. Plant Physiol. 117, 1393–1400. Borse, B.B., Jagan Mohan Rao, L., Nagalakshmi, S. and Krishnamurthy, N. (2002) Fingerprint of black teas from India: identification of the regio-specific characteristics. Food Chem. 79, 419–424. Brash, A.R. (2009) Mechanistic aspects of CYP74 allene oxide synthases and related cytochrome P450 enzymes. Phytochemistry, 70, 1522–1531. Brilli, F., Ruuskanen, T.M., Schnitzhofer, R., Muller, M., Breitenlechner, M., Bittner, V., Wohlfahrt, G., Loreto, F. and Hansel, A. (2011) Detection of plant volatiles after leaf wounding and darkening by proton transfer reaction “time-of-flight” mass spectrometry (PTR-TOF). PLoS ONE, 6, e20419. Broekgaarden, C., Snoeren, T.A., Dicke, M. and Vosman, B. (2011) Exploiting natural variation to identify insect-resistance genes. Plant Biotechnol. J. 9, 819–825. Buchhaupt, M., Guder, J.C., Etschmann, M.M.W. and Schrader, J. (2012) Synthesis of green note aroma compounds by biotransformation of fatty acids using yeast cells coexpressing lipoxygenase and hydroperoxide lyase. Appl. Microbiol. Biotechnol. 93, 159–168. Cacas, J.-L., Vailleau, F., Davoine, C., Ennar, N., Agnel, J.-P., Tronchet, M., Ponchet, M., Blein, J.-P., Roby, D., Triantaphylides, C. and Montillet, J.-L. (2005) The combined action of 9 lipoxygenase and galactolipase is sufficient to bring about programmed cell death during tobacco hypersensitive response. Plant Cell Environ. 28, 1367–1378. Chehab, E.W., Raman, G., Walley, J.W., Perea, J.V., Banu, G., Theg, S. and Dehesh, K. (2006) Rice HYDROPEROXIDE LYASES with unique expression patterns generate distinct aldehyde signatures in Arabidopsis. Plant Physiol. 141, 121–134. Chehab, E.W., Kaspi, R., Savchenko, T., Rowe, H., Negre-Zakharov, F., Kliebenstein, D. and Dehesh, K. (2008) Distinct roles of jasmonates and aldehydes in plant-defense responses. PLoS ONE, 3, e1904. Chohany, L.E., Bishop, K.A., Camic, H., Sup, S.J., Findeis, P.M. and Clapp, C.H. (2011) Cationic substrates of soybean lipoxygenase-1. Bioorg. Chem. 39, 94– 100. Christensen, S.A., Nemchenko, A., Borrego, E., Murray, I., Sobhy, I.S., Bosak, L., DeBlasio, S., Erb, M., Robert, C.A. and Vaughn, K.A. (2013) The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack. Plant J. 74, 59–73. Croft, K., Juttner, F. and Slusarenko, A.J. (1993) Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol. 101, 13–24. D’Auria, J.C., Pichersky, E., Schaub, A., Hansel, A. and Gershenzon, J. (2007) Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J. 49, 194–207. De Domenico, S., Tsesmetzis, N., Di Sansebastiano, G.P., Hughes, R.K., Casey, R. and Santino, A. (2007) Subcellular localisation of Medicago truncatula 9/ 13-hydroperoxide lyase reveals a new localisation pattern and activation mechanism for CYP74C enzymes. BMC Plant Biol. 7, 58. De Vleesschauwer, D., Gheysen, G. and Hofte, M. (2013) Hormone defense networking in rice: tales from a different world. Trends Plant Sci. 18, 555– 565. Delcarte, J., Fauconnier, M., Jacques, P., Matsui, K., Thonart, P. and Marlier, M. (2003) Optimisation of expression and immobilized metal ion affinity chromatographic purification of recombinant (His)6-tagged cytochrome P450 hydroperoxide lyase in Escherichia coli. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 786, 229–236. Derksen, H., Rampitsch, C. and Daayf, F. (2013) Signaling cross-talk in plant disease resistance. Plant Sci. 207, 79–87. D’Haeze, W. and Holsters, M. (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology, 12, 79R– 105R. Du, X., Plotto, A., Baldwin, E. and Rouseff, R. (2011) Evaluation of volatiles from two subtropical strawberry cultivars using GC-olfactometry, GC-MS odor activity values, and sensory analysis. J. Agric. Food Chem. 59, 12569– 12577. Engelberth, J., Alborn, H.T., Schmelz, E.A. and Tumlinson, J.H. (2004) Airborne signals prime plants against insect herbivore attack. Proc. Natl Acad. Sci. U.S.A. 101, 1781–1785. Engelberth, J., Seidl-Adams, I., Schultz, J.C. and Tumlinson, J.H. (2007) Insect elicitors and exposure to green leafy volatiles differentially upregulate major octadecanoids and transcripts of 12-oxo phytodienoic acid reductases in Zea mays. Mol. Plant Microbe Interact. 20, 707–716. Engelberth, J., Contreras, C.F., Dalvi, C., Li, T. and Engelberth, M. (2013) Early transcriptome analyses of Z-3-Hexenol-treated zea mays revealed distinct transcriptional networks and anti-herbivore defense potential of green leaf volatiles. PLoS ONE, 8, e77465. Erb, M., Meldau, S. and Howe, G.A. (2012) Role of phytohormones in insectspecific plant reactions. Trends Plant Sci. 17, 250–259. Fall, R., Karl, T., Hansel, A., Jordan, A. and Lindinger, W. (1999) Volatile organic compounds emitted after leaf wounding: on-line analysis by protontransfer-reaction mass spectrometry. J. Geophys. Res. Atmos. 104, 15963– 15974. Farag, M.A., Fokar, M., Abd, H., Zhang, H., Allen, R.D. and Pare, P.W. (2005) (Z)-3-Hexenol induces defense genes and downstream metabolites in maize. Planta, 220, 900–909. Farmaki, T., Sanmartın, M., Jimenez, P., Paneque, M., Sanz, C., Vancanneyt, G., n, J. and Sanchez-Serrano, J.J. (2007) Differential distribution of the Leo lipoxygenase pathway enzymes within potato chloroplasts. J. Exp. Bot. 58, 555–568. Farmer, E.E. and Mueller, M.J. (2013) ROS-mediated lipid peroxidation and RESactivated signaling. Annu. Rev. Plant Biol. 64, 429–450. Farmer, E.E., Almeras, E. and Krishnamurthy, V. (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr. Opin. Plant Biol. 6, 372–378. Fauconnier, M.L., Mpambara, A., Delcarte, J., Jacques, P., Thonart, P. and Marlier, M. (1999) Conversion of green note aldehydes into alcohols by yeast alcohol dehydrogenase. Biotechnol. Lett. 21, 629–633. Feussner, I. and Wasternack, C. (2002) The lipoxygenase pathway. Annu. Rev. Plant Biol. 53, 275–297. Froehlich, J.E., Itoh, A. and Howe, G.A. (2001) Tomato allene oxide synthase and fatty acid hydroperoxide lyase, two cytochrome P450s involved in ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739 736 Muhammad Naeem ul Hassan et al. oxylipin metabolism, are targeted to different membranes of chloroplast envelope. Plant Physiol. 125, 306–317. Frost, C.J., Mescher, M.C., Carlson, J.E. and De Moraes, C.M. (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol. 146, 818–824. Frydman, A., Weisshaus, O., Bar-Peled, M., Huhman, D.V., Sumner, L.W., Marin, F.R., Lewinsohn, E., Fluhr, R., Gressel, J. and Eyal, Y. (2004) Citrus fruit bitter flavors: isolation and functional characterization of the gene Cm1,2RhaT encoding a 1,2 rhamnosyltransferase, a key enzyme in the biosynthesis of the bitter flavonoids of citrus. Plant J. 40, 88–100. Fukushige, H. and Hildebrand, D.F. (2005) Watermelon (Citrullus lanatus) hydroperoxide lyase greatly increases C6 aldehyde formation in transgenic leaves. J. Agric. Food Chem. 53, 2046–2051. Galliard, T., Phillips, D.R. and Reynolds, J. (1976) The formation of cis-3nonenal, trans-2-nonenal and hexanal from linoleic acid hydroperoxide isomers by a hydroperoxide cleavage enzyme system in cucumber (Cucumis sativus) fruits. Biochim. Biophys. Acta, 441, 181–192. Gao, X., Shim, W.B., Gobel, C., Kunze, S., Feussner, I., Meeley, R., Balint-Kurti, P. and Kolomiets, M. (2007) Disruption of a maize 9-lipoxygenase results in increased resistance to fungal pathogens and reduced levels of contamination with mycotoxin fumonisin. Mol. Plant Microbe Interact. 20, 922–933. Gao, X., Starr, J., Gobel, C., Engelberth, J., Feussner, I., Tumlinson, J. and Kolomiets, M. (2008) Maize 9-lipoxygenase ZmLOX3 controls development, root-specific expression of defense genes, and resistance to root-knot nematodes. Mol. Plant Microbe Interact. 21, 98–109. Gershenzon, J. (2007) Plant volatiles carry both public and private messages. Proc. Natl Acad. Sci. U.S.A. 104, 5257–5258. Gigot, C., Ongena, M., Fauconnier, M.-L., Wathelet, J.-P., Du Jardin, P. and Thonart, P. (2010) The lipoxygenase metabolic pathway in plants: potential for industrial production of natural green leaf volatiles. Biotechnol. Agron. Soc. Environ. 14, 451–460. Gigot, C., Ongena, M., Fauconnier, M.-L., Muhovski, Y., Wathelet, J.-P., du Jardin, P. and Thonart, P. (2012) Optimization and scaling up of a biotechnological synthesis of natural green leaf volatiles using Beta vulgaris hydroperoxide lyase. Process Biochem. 47, 2547–2551. Gobel, C., Feussner, I. and Rosahl, S. (2003) Lipid peroxidation during the hypersensitive response in potato in the absence of 9-lipoxygenases. J. Biol. Chem. 278, 52834–52840. Goellner, K. and Conrath, U. (2008) Priming: it’s all the world to induced disease resistance. Eur. J. Plant Pathol. 121, 233–242. Goff, S.A. and Klee, H.J. (2006) Plant volatile compounds: sensory cues for health and nutritional value? Science, 311, 815–819. Gomi, K., Yamasaki, Y., Yamamoto, H. and Akimitsu, K. (2003) Characterization of a hydroperoxide lyase gene and effect of C6-volatiles on expression of genes of the oxylipin metabolism in Citrus. J. Plant Physiol. 160, 1219–1231. Gomi, K., Satoh, M., Ozawa, R., Shinonaga, Y., Sanada, S., Sasaki, K., Matsumura, M., Ohashi, Y., Kanno, H., Akimitsu, K. and Takabayashi, J. (2010) Role of hydroperoxide lyase in white-backed planthopper (Sogatella furcifera Horvath)-induced resistance to bacterial blight in rice, Oryza sativa L. Plant J. 61, 46–57. €bel, C., Francis, F., Haubruge, E., Wathelet, J.-P., Du Gosset, V., Harmel, N., Go Jardin, P., Feussner, I. and Fauconnier, M.-L. (2009) Attacks by a piercingsucking insect (Myzus persicae Sultzer) or a chewing insect (Leptinotarsa decemlineata Say) on potato plants (Solanum tuberosum L.) induce differential changes in volatile compound release and oxylipin synthesis. J. Exp. Bot. 60(4), 1231–40, erp015. Graner, G., Hamberg, M. and Meijer, J. (2003) Screening of oxylipins for control of oilseed rape (Brassica napus) fungal pathogens. Phytochemistry, 63, 89– 95. Grechkin, A.N. and Hamberg, M. (2004) The “heterolytic hydroperoxide lyase” is an isomerase producing a short-lived fatty acid hemiacetal. Biochim. Biophys. Acta, 1636, 47–58. Grechkin, A.N., Bruhlmann, F., Mukhtarova, L.S., Gogolev, Y.V. and Hamberg, M. (2006) Hydroperoxide lyases (CYP74C and CYP74B) catalyze the homolytic isomerization of fatty acid hydroperoxides into hemiacetals. Biochim. Biophys. Acta, 1761, 1419–1428. €m, J.Z. and Funk, C.D. (2011) Lipoxygenase and leukotriene Haeggstro pathways: biochemistry, biology, and roles in disease. Chem. Rev. 111, 5866–5898. Halitschke, R. and Baldwin, I.T. (2003) Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J. 36, 794–807. Halitschke, R., Stenberg, J.A., Kessler, D., Kessler, A. and Baldwin, I.T. (2008) Shared signals –‘alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecol. Lett. 11, 24–34. Hatanaka, A. (1993) The biogeneration of green odour by green leaves. Phytochemistry, 34, 1201–1218. Heiden, A.C., Kobel, K., Langebartels, C., Schuh-Thomas, G. and Wildt, J. (2003) Emissions of oxygenated volatile organic compounds from plants part I: emissions from lipoxygenase activity. J. Atmos. Chem. 45, 143–172. Heil, M. (2014) Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytol. 204, 297–306. Heil, M. and Kost, C. (2006) Priming of indirect defences. Ecol. Lett. 9, 813–817. Heil, M. and Silva Bueno, J.C. (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl Acad. Sci. U.S.A. 104, 5467–5472. €nsche, H., Fang, J., Baldwin, I.T. Heinrich, M., Hettenhausen, C., Lange, T., Wu and Wu, J. (2013) High levels of jasmonic acid antagonize the biosynthesis of gibberellins and inhibit the growth of Nicotiana attenuata stems. Plant J. 73, 591–606. Hirao, T., Okazawa, A., Harada, K., Kobayashi, A., Muranaka, T. and Hirata, K. (2012) Green leaf volatiles enhance methyl jasmonate response in Arabidopsis. J. Biosci. Bioeng. 114, 540–545. Huang, F.C. and Schwab, W. (2011) Cloning and characterization of a 9lipoxygenase gene induced by pathogen attack from Nicotiana benthamiana for biotechnological application. BMC Biotechnol. 11, 30. Huang, F.C. and Schwab, W. (2012) Overexpression of hydroperoxide lyase, peroxygenase and epoxide hydrolase in tobacco for the biotechnological production of flavours and polymer precursors. Plant Biotechnol. J. 10, 1099– 1109. Huang, F.C., Studart-Witkowski, C. and Schwab, W. (2010) Overexpression of hydroperoxide lyase gene in Nicotiana benthamiana using a viral vector system. Plant Biotechnol. J. 8, 783–795. Hubert, J., Munzbergova, Z., Nesvorna, M., Poltronieri, P. and Santino, A. (2008) Acaricidal effects of natural six-carbon and nine-carbon aldehydes on stored-product mites. Exp. Appl. Acarol. 44, 315–321. Hughes, R.K., De Domenico, S. and Santino, A. (2009) Plant cytochrome CYP74 family: biochemical features, endocellular localisation, activation mechanism in plant defence and improvements for industrial applications. ChemBioChem, 10, 1122–1133. Hwang, I.S. and Hwang, B.K. (2010) The pepper 9-lipoxygenase gene CaLOX1 functions in defense and cell death responses to microbial pathogens. Plant Physiol. 152, 948–967. Hyun, Y., Choi, S., Hwang, H.-J., Yu, J., Nam, S.-J., Ko, J., Park, J.-Y., Seo, Y.S., Kim, E.Y., Ryu, S.B., Kim, W.T., Lee, Y.-H., Kang, H. and Lee, I. (2008) Cooperation and functional diversification of two closely related galactolipase genes for jasmonate biosynthesis. Dev. Cell, 14, 183–192. Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I. and Okada, K. (2001) The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell, 13, 2191–2209. Jalloul, A., Montillet, J.L., Assigbetse, K., Agnel, J.P., Delannoy, E., Triantaphylides, C., Daniel, J.F., Marmey, P., Geiger, J.P. and Nicole, M. (2002) Lipid peroxidation in cotton: Xanthomonas interactions and the role of lipoxygenases during the hypersensitive reaction. Plant J. 32, 1–12. Joo, Y.-C. and Oh, D.-K. (2012) Lipoxygenases: potential starting biocatalysts for the synthesis of signaling compounds. Biotechnol. Adv. 30, 1524–1532. Kaplan, I. (2012) Attracting carnivorous arthropods with plant volatiles: the future of biocontrol or playing with fire? Biol. Control, 60, 77–89. Kessler, A., Halitschke, R. and Baldwin, I.T. (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science, 305, 665– 668. ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739 GLVs functions and their applications 737 Kessler, A., Halitschke, R., Diezel, C. and Baldwin, I.T. (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia, 148, 280–292. Kishimoto, K., Matsui, K., Ozawa, R. and Takabayashi, J. (2008) Direct fungicidal activities of C6-aldehydes are important constituents for defense responses in Arabidopsis against Botrytis cinerea. Phytochemistry, 69, 2127– 2132. Kolomiets, M.V., Hannapel, D.J., Chen, H., Tymeson, M. and Gladon, R.J. (2001) Lipoxygenase is involved in the control of potato tuber development. Plant Cell, 13, 613–626. Lang, I., Gobel, C., Porzel, A., Heilmann, I. and Feussner, I. (2008) A lipoxygenase with linoleate diol synthase activity from Nostoc sp. PCC 7120. Biochem. J. 410, 347–357. Lange, B.M. and Ahkami, A. (2013) Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes–current status and future opportunities. Plant Biotechnol. J. 11, 169–196. , R.M., Fuentes, T., Sayez, G., Graell, J. and Lo pez, M.L. (2003) Lara, I., Miro Biosynthesis of volatile aroma compounds in pear fruit stored under longterm controlled-atmosphere conditions. Postharvest Biol. Technol. 29, 29–39. Li, Y., Zhong, S., Qin, Y., Zhang, S., Gao, Z., Dang, Z. and Pan, W. (2014) Identification of plant chemicals attracting and repelling whiteflies. Arthropod Plant Interact. 8, 183–190. Liavonchanka, A. and Feussner, I. (2006) Lipoxygenases: occurrence, functions and catalysis. J. Plant Physiol. 163, 348–357. Liechti, R. and Farmer, E.E. (2003) The Jasmonate Biochemical Pathway. Liechti, R. and Farmer, E.E. (2006) Jasmonate Biochemical Pathway. Liechti, R., Gfeller, A. and Farmer, E.E. (2006) Jasmonate Signaling Pathway. Liu, X., Li, F., Tang, J., Wang, W., Zhang, F., Wang, G., Chu, J., Yan, C., Wang, T., Chu, C. and Li, C. (2012) Activation of the jasmonic acid pathway by depletion of the hydroperoxide lyase OsHPL3 reveals crosstalk between the HPL and AOS branches of the oxylipin pathway in rice. PLoS ONE, 7, e50089. Lyons, R., Manners, J.M. and Kazan, K. (2013) Jasmonate biosynthesis and signaling in monocots: a comparative overview. Plant Cell Rep. 32, 815–827. Marmey, P., Jalloul, A., Alhamdia, M., Assigbetse, K., Cacas, J.L., Voloudakis, A.E., Champion, A., Clerivet, A., Montillet, J.L. and Nicole, M. (2007) The 9lipoxygenase GhLOX1 gene is associated with the hypersensitive reaction of cotton Gossypium hirsutum to Xanthomonas campestris pv malvacearum. Plant Physiol. Biochem. 45, 596–606. Matsui, K. (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin metabolism. Curr. Opin. Plant Biol. 9, 274–280. Matsui, K., Ujita, C., Fujimoto, S., Wilkinson, J., Hiatt, B., Knauf, V., Kajiwara, T. and Feussner, I. (2000) Fatty acid 9- and 13-hydroperoxide lyases from cucumber. FEBS Lett. 481, 183–188. Matsui, K., Minami, A., Hornung, E., Shibata, H., Kishimoto, K., Ahnert, V., Kindl, H., Kajiwara, T. and Feussner, I. (2006) Biosynthesis of fatty acid derived aldehydes is induced upon mechanical wounding and its products show fungicidal activities in cucumber. Phytochemistry, 67, 649–657. Meldau, S., Erb, M. and Baldwin, I.T. (2012) Defence on demand: mechanisms behind optimal defence patterns. Ann. Bot. 110, 1503–1514. von M erey, G.E., Veyrat, N., D’Alessandro, M. and Turlings, T.C. (2013) Herbivore-induced maize leaf volatiles affect attraction and feeding behavior of Spodoptera littoralis caterpillars. Front. Plant Sci. 4:209. doi: 10.3389/ fpls.2013.00209. Mita, G., Quarta, A., Fasano, P., De Paolis, A., Di Sansebastiano, G.P., Perrotta, C., Iannacone, R., Belfield, E., Hughes, R., Tsesmetzis, N., Casey, R. and Santino, A. (2005) Molecular cloning and characterization of an almond 9hydroperoxide lyase, a new CYP74 targeted to lipid bodies. J. Exp. Bot. 56, 2321–2333. Mita, G., Fasano, P., De Domenico, S., Perrone, G., Epifani, F., Iannacone, R., Casey, R. and Santino, A. (2007) 9-Lipoxygenase metabolism is involved in the almond/Aspergillus carbonarius interaction. J. Exp. Bot. 58, 1803–1811. Morant, M., Bak, S., Moller, B.L. and Werck-Reichhart, D. (2003) Plant cytochromes P450: tools for pharmacology, plant protection and phytoremediation. Curr. Opin. Biotechnol. 14, 151–162. Mu, W., Xue, Q., Jiang, B. and Hua, Y. (2012) Molecular cloning, expression, and enzymatic characterization of Solanum tuberosum hydroperoxide lyase. Eur. Food Res. Technol. 234, 723–731. Myung, K., Hamilton-Kemp, T.R. and Archbold, D.D. (2007) Interaction with and effects on the profile of proteins of Botrytis cinerea by C6 aldehydes. J. Agric. Food Chem. 55, 2182–2188. Nakamura, S. and Hatanaka, A. (2002) Green-leaf-derived C6-aroma compounds with potent antibacterial action that act on both Gramnegative and Gram-positive bacteria. J. Agric. Food Chem. 50, 7639–7644. € K€annaste, A. and Copolovici, L. (2013) Quantitative patterns Niinemets, U., between plant volatile emissions induced by biotic stresses and the degree of damage. Front. Plant Sci. 4:262. doi: 10.3389/fpls.2013.00262. Noordermeer, M.A., Van Dijken, A.J., Smeekens, S.C., Veldink, G.A. and Vliegenthart, J.F. (2000) Characterization of three cloned and expressed 13hydroperoxide lyase isoenzymes from alfalfa with unusual N-terminal sequences and different enzyme kinetics. Eur J Biochem. 267(9), 2473–82. Noordermeer, M.A., Veldink, G.A. and Vliegenthart, J.F. (2001) Fatty acid hydroperoxide lyase: a plant cytochrome p450 enzyme involved in wound healing and pest resistance. ChemBioChem, 2, 494–504. Oliveira, I., Guedes de Pinho, P., Malheiro, R., Baptista, P. and Pereira, J.A. (2011) Volatile profile of Arbutus unedo L. fruits through ripening stage. Food Chem. 128, 667–673. Panagakou, I., Touloupakis, E. and Ghanotakis, D.F. (2013) Structural characterization of hydroperoxide lyase in dodecyl maltoside by using circular dichroism. Protein J. 32, 1–6. Park, Y.S., Kunze, S., Ni, X., Feussner, I. and Kolomiets, M.V. (2010) Comparative molecular and biochemical characterization of segmentally duplicated 9-lipoxygenase genes ZmLOX4 and ZmLOX5 of maize. Planta, 231, 1425–1437. Porta, H., Figueroa-Balderas, R. and Rocha-Sosa, M. (2008) Wounding and pathogen infection induce a chloroplast-targeted lipoxygenase in the common bean (Phaseolus vulgaris L.). Planta, 227, 363–373. Prost, I., Dhondt, S., Rothe, G., Vicente, J., Rodriguez, M.J., Kift, N., Carbonne, F., Griffiths, G., Esquerre-Tugaye, M.-T. and Rosahl, S. (2005) Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiol. 139, 1902–1913. Rance, I., Fournier, J. and Esquerre-Tugaye, M.T. (1998) The incompatible interaction between Phytophthora parasitica var. nicotianae race 0 and tobacco is suppressed in transgenic plants expressing antisense lipoxygenase sequences. Proc. Natl Acad. Sci. U.S.A. 95, 6554–6559. Rudolph, M., Schlereth, A., Korner, M., Feussner, K., Berndt, E., Melzer, M., Hornung, E. and Feussner, I. (2011) The lipoxygenase-dependent oxygenation of lipid body membranes is promoted by a patatin-type phospholipase in cucumber cotyledons. J. Exp. Bot. 62, 749–760. Rusterucci, C., Montillet, J.L., Agnel, J.P., Battesti, C., Alonso, B., Knoll, A., Bessoule, J.J., Etienne, P., Suty, L., Blein, J.P. and Triantaphylides, C. (1999) Involvement of lipoxygenase-dependent production of fatty acid hydroperoxides in the development of the hypersensitive cell death induced by cryptogein on tobacco leaves. J. Biol. Chem. 274, 36446–36455. Ryu, S.B. (2004) Phospholipid-derived signaling mediated by phospholipase A in plants. Trends Plant Sci. 9, 229–235. mez, M.P., Kermasha, S., Nicaud, J.-M., Belin, J.-M. and Husson, F. Santiago-Go (2010) Predicted secondary structure of hydroperoxide lyase from green bell pepper cloned in the yeast Yarrowia lipolytica. J. Mol. Catal. B Enzym. 65, 63– 67. Sayegh-Alhamdia, M., Marmey, P., Jalloul, A., Champion, A., Petitot, A.S., Clerivet, A. and Nicole, M. (2008) Association of lipoxygenase response with resistance of various cotton genotypes to the bacterial blight disease. J. Phytopathol. 156, 542–549. Scala, A., Allmann, S., Mirabella, R., Haring, M. and Schuurink, R. (2013a) Green leaf volatiles: a plant’s multifunctional weapon against herbivores and pathogens. Int. J. Mol. Sci. 14, 17781–17811. Scala, A., Mirabella, R., Mugo, C., Matsui, K., Haring, M.A. and Schuurink, R.C. (2013b) E-2-hexenal promotes susceptibility to Pseudomonas syringae by activating jasmonic acid pathways in Arabidopsis. Front. Plant Sci. 4:74. doi: 10.3389/fpls.2013.00074. Schaller, A. and Stintzi, A. (2009) Enzymes in jasmonate biosynthesis – structure, function, regulation. Phytochemistry, 70, 1532–1538. Scherer, G.F.E., Ryu, S.B., Wang, X., Matos, A.R. and Heitz, T. (2010) Patatinrelated phospholipase A: nomenclature, subfamilies and functions in plants. Trends Plant Sci. 15, 693–700. ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739 738 Muhammad Naeem ul Hassan et al. Schilmiller, A.L., Last, R.L. and Pichersky, E. (2008) Harnessing plant trichome biochemistry for the production of useful compounds. Plant J. 54, 702–711. Schneider, C., Pratt, D.A., Porter, N.A. and Brash, A.R. (2007) Control of oxygenation in lipoxygenase and cyclooxygenase catalysis. Chem. Biol. 14, 473–488. Schuh, C. and Schieberle, P. (2006) Characterization of the key aroma compounds in the beverage prepared from Darjeeling black tea: quantitative differences between tea leaves and infusion. J. Agric. Food Chem. 54, 916– 924. Selli, S., Kelebek, H., Ayseli, M.T. and Tokbas, H. (2014) Characterization of the most aroma-active compounds in cherry tomato by application of the aroma extract dilution analysis. Food Chem. 165, 540–546. Seymour, G.B., Chapman, N.H., Chew, B.L. and Rose, J.K. (2013) Regulation of ripening and opportunities for control in tomato and other fruits. Plant Biotechnol. J. 11, 269–278. Shang, W., Ivanov, I., Svergun, D.I., Borbulevych, O.Y., Aleem, A.M., Stehling, €hn, H. and Skrzypczak-Jankun, E. (2011) Probing S., Jankun, J., Ku dimerization and structural flexibility of mammalian lipoxygenases by smallangle X-ray scattering. J. Mol. Biol. 409, 654–668. Shin, J.H., Van, K., Kim, D.H., Kim, K.D., Jang, Y.E., Choi, B.-S., Kim, M.Y. and Lee, S.-H. (2008) The lipoxygenase gene family: a genomic fossil of shared polyploidy between Glycine max and Medicago truncatula. BMC Plant Biol. 8, 133. Shiojiri, K., Kishimoto, K., Ozawa, R., Kugimiya, S., Urashimo, S., Arimura, G., Horiuchi, J., Nishioka, T., Matsui, K. and Takabayashi, J. (2006a) Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc. Natl Acad. Sci. U.S.A. 103, 16672–16676. Shiojiri, K., Ozawa, R., Matsui, K., Kishimoto, K., Kugimiya, S. and Takabayashi, J. (2006b) Role of the lipoxygenase/lyase pathway of host-food plants in the host searching behavior of two parasitoid species, Cotesia glomerata and Cotesia plutellae. J. Chem. Ecol. 32, 969–979. Shiojiri, K., Ozawa, R., Matsui, K., Sabelis, M.W. and Takabayashi, J. (2012) Intermittent exposure to traces of green leaf volatiles triggers a plant response. Sci. Rep. 2:378. doi: 10.1038/srep00378. Siedow, J.N. (1991) Plant lipoxygenase: structure and function. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 145–188. Steinhaus, M., Sinuco, D., Polster, J., Osorio, C. and Schieberle, P. (2009) Characterization of the key aroma compounds in pink guava (Psidium guajava L.) by means of aroma re-engineering experiments and omission tests. J. Agric. Food Chem. 57, 2882–2888. Sujatha, B., Devi, P. and Maheswari, U. (2012) Antifungal potential of papaya lipoxygenase metabolites against Phytophthora palmivora. J. Pure Appl. Microbiol. 6, 433–438. Tijet, N. and Brash, A.R. (2002) Allene oxide synthases and allene oxides. Prostaglandins Other Lipid Mediat. 68–69, 423–431. Ton, J., D’Alessandro, M., Jourdie, V., Jakab, G., Karlen, D., Held, M., MauchMani, B. and Turlings, T.C. (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J. 49, 16–26. Tong, X., Qi, J., Zhu, X., Mao, B., Zeng, L., Wang, B., Li, Q., Zhou, G., Xu, X. and Lou, Y. (2012) The rice hydroperoxide lyase OsHPL3 functions in defense responses by modulating the oxylipin pathway. Plant J. 71, 763–775. Turlings, T.C., Loughrin, J.H., McCall, P.J., Rose, U.S., Lewis, W.J. and Tumlinson, J.H. (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc. Natl Acad. Sci. U.S.A. 92, 4169–4174. D., Nikicevic, N.J., Zivkovic, Velickovic, M.M., Radivojevic, D.D., Oparnica, C. M.B., Dordevi c, N.O., Vajs, V.E. and Tesevic, V.V. (2013) Volatile compounds in Medlar fruit (Mespilus germanica L.) at two ripening stages. Hemijska industrija, 67, 437–441. Vellosillo, T., Martinez, M., Lopez, M.A., Vicente, J., Cascon, T., Dolan, L., Hamberg, M. and Castresana, C. (2007) Oxylipins produced by the 9lipoxygenase pathway in Arabidopsis regulate lateral root development and defense responses through a specific signaling cascade. Plant Cell, 19, 831– 846. Verdonk, J.C., Ric de Vos, C.H., Verhoeven, H.A., Haring, M.A., van Tunen, A.J. and Schuurink, R.C. (2003) Regulation of floral scent production in petunia revealed by targeted metabolomics. Phytochemistry, 62, 997–1008. Vernooy-Gerritsen, M., Leunissen, J.L.M., Veldink, G.A. and Vliegenthart, J.F.G. (1984) Intracellular localization of lipoxygenases-1 and -2 in germinating soybean seeds by indirect labeling with protein A-colloidal gold complexes. Plant Physiol. 76, 1070–1078. Vicente, J., Cascon, T., Vicedo, B., Garcia-Agustin, P., Hamberg, M. and Castresana, C. (2012) Role of 9-lipoxygenase and alpha-dioxygenase oxylipin pathways as modulators of local and systemic defense. Mol. Plant, 5, 914– 928. Vieira, C.R., Blassioli-Moraes, M.C., Borges, M., Pires, C.S.S., Sujii, E.R. and Laumann, R.A. (2014) Field evaluation of (E)-2-hexenal efficacy for behavioral manipulation of egg parasitoids in soybean. Biocontrol, 59, 525–537. Vogt, J., Schiller, D., Ulrich, D., Schwab, W. and Dunemann, F. (2013) Identification of lipoxygenase (LOX) genes putatively involved in fruit flavour formation in apple (Malus 9 domestica). Tree Genet. Genomes, 9, 1493– 1511. €hn, H. (2011) The Walther, M., Hofheinz, K., Vogel, R., Roffeis, J. and Ku N-terminal b-barrel domain of mammalian lipoxygenases including mouse 5-lipoxygenase is not essential for catalytic activity and membrane binding but exhibits regulatory functions. Arch. Biochem. Biophys. 516, 1–9. Wan, X.H., Chen, S.X., Wang, C.Y., Zhang, R.R., Cheng, S.Q., Meng, H.W. and Shen, X.Q. (2013) Isolation, expression, and characterization of a hydroperoxide lyase gene from cucumber. Int. J. Mol. Sci. 14, 22082–22101. Wang, K., Liu, F., Liu, Z., Huang, J., Xu, Z., Li, Y., Chen, J., Gong, Y. and Yang, X. (2011) Comparison of catechins and volatile compounds among different types of tea using high performance liquid chromatograph and gas chromatograph mass spectrometer. Int. J. Food Sci. Technol. 46, 1406– 1412. Wang, B., Zhou, G., Xin, Z., Ji, R. and Lou, Y. (2014) (Z)-3-hexenal, one of the green leaf volatiles, increases susceptibility of rice to the white-backed planthopper Sogatella furcifera. Plant Mol. Biol. Rep. doi: 10.1007/s11105014-0756-7. Wasternack, C. (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. 100, 681–697. Wasternack, C. and Hause, B. (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 111, 1021–1058. Wei, J., Wang, L., Zhu, J., Zhang, S., Nandi, O.I. and Kang, L. (2007) Plants attract parasitic wasps to defend themselves against insect pests by releasing hexenol. PLoS ONE, 2, e852. Weichert, H., Kolbe, A., Kraus, A., Wasternack, C. and Feussner, I. (2002) Metabolic profiling of oxylipins in germinating cucumber seedlings– lipoxygenase-dependent degradation of triacylglycerols and biosynthesis of volatile aldehydes. Planta, 215, 612–619. Xin, Z., Zhang, L., Zhang, Z., Chen, Z. and Sun, X. (2014) A tea hydroperoxide lyase gene, CsiHPL1, regulates tomato defense response against Prodenia litura (Fabricius) and Alternaria alternata f. sp. Lycopersici by modulating green leaf volatiles (GLVs) release and jasmonic acid (JA) gene expression. Plant Mol. Biol. Rep. 32, 62–69. Xiong, J., Kong, X., Zhang, C., Chen, Y. and Hua, Y. (2012) Production of (2E)hexenal by a hydroperoxide lyase from Amaranthus tricolor and salt-adding steam distillation for the separation. Eur. Food Res. Technol. 235, 783–792. Xu, P., Hua, D. and Ma, C. (2007) Microbial transformation of propenylbenzenes for natural flavour production. Trends Biotechnol. 25, 571–576. Yan, Z.-G. and Wang, C.-Z. (2006) Wound-induced green leaf volatiles cause the release of acetylated derivatives and a terpenoid in maize. Phytochemistry, 67, 34–42. Yang, W.-Y., Zheng, Y., Bahn, S.C., Pan, X.-Q., Li, M.-Y., Vu, H.S., Roth, M.R., Scheu, B., Welti, R., Hong, Y.-Y. and Wang, X.-M. (2012a) The patatincontaining phospholipase A pPLAIIa modulates oxylipin formation and water loss in Arabidopsis thaliana. Mol. Plant, 5(2), 452–60 doi: 10.1093/mp/ ssr118. Yang, X.-Y., Jiang, W.-J. and Yu, H.-J. (2012b) The expression profiling of the lipoxygenase (LOX) family genes during fruit development, abiotic stress and ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739 GLVs functions and their applications 739 hormonal treatments in cucumber (Cucumis sativus L.). Int. J. Mol. Sci. 13, 2481–2500. Yang, D.L., Yang, Y. and He, Z. (2013) Roles of plant hormones and their interplay in rice immunity. Mol. Plant, 6, 675–685. Yi, H.S., Heil, M., Adame-Alvarez, R.M., Ballhorn, D.J. and Ryu, C.M. (2009) Airborne induction and priming of plant defenses against a bacterial pathogen. Plant Physiol. 151, 2152–2161. Zheng, Y. and Brash, A.R. (2010) On the role of molecular oxygen in lipoxygenase activation: comparison and contrast of epidermal lipoxygenase3 with soybean lipoxygenase-1. J. Biol. Chem. 285, 39876–39887. Zhu, B.Q., Xu, X.Q., Wu, Y.W., Duan, C.Q. and Pan, Q.H. (2012) Isolation and characterization of two hydroperoxide lyase genes from grape berries: HPL isogenes in Vitis vinifera grapes. Mol. Biol. Rep. 39, 7443–7455. ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739